RESEARCH

Ancient Termite Pollinator of Milkweed Flowers in Dominican Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021

GEORGE O. POINAR, JR.

hen we think of pollinators, bees are the first things considered separate families, rather than subfamilies included that come to mind. However, there are many other within the . While the overlap in morphological Wless obvious pollinators in the insect world, many of structure of the pollinia in these groups can be similar, the which pollinate tropical flowers we never knew existed. When we manner by which they attach their pollinaria to the pollinator think of termites, the first thing that comes to mind is the terrible differs. While the orchids typically attach their pollinaria by a damage they can do to our homes. We never think of termites sticky pad (viscidium) (Dressler 1993; Poinar 2016a, 2016b), the as visiting flowers and especially not pollinating them, which milkweeds normally use a slender, more or less rigid structure makes the present discovery so interesting. Embedded in a piece called a corpusculum that is usually sutured along the outer of Dominican amber is a harvester termite (Isoptera: Termitidae) surface, but smooth on the inner surface, to attach their pol- with a pollinarium from an adjacent milkweed flower attached linia to insects (Swarupanandan et al. 1996)(Fig. 1). Milkweed to its head. Such an association is completely unknown today. pollinia and pollinaria vary in structure among different ascle- Currently, there are two major families that distribute piad lineages: pollinia of the common milkweed, their in little sacs called pollinia for attachment to insects: syriaca L., which are often found attached to the mouthparts orchids (Orchidoideae and Epidendroideae) and milkweeds of honeybees, are rather slender, while others such as the (Asclepiadoideae). Also possessing pollinia are members of pollinia attached to the termite are more swollen. the Periplocoideae and Secamonoideae, if those lineages are The fossil termite adjacent to the milkweed flower in Domini- can amber carries pollinia that match those found in the stigmat- ic cavity of the flower, thus establishing termites as pollinators of ancient lineages of the Asclepiadoideae in the mid-Tertiary. The flower, which represents the first fossil milkweed flower, is described below, and ways in which the termite may have acquired the pollinia are discussed.

Materials and Methods The fossil flower originated from amber mines in the northern mountain range (Cordillera Septentrional) of the Dominican Republic between Puerto Plata and Santiago. Amber from mines in this region was produced by protera Poinar (1991) (), and based on the recovered biota, the origi- nal habitat was characterized as a tropical moist forest (Poinar and Poinar 1999). Ages range from 20–15 mya based on Foraminifera (Itur- ralde-Vinent and MacPhee 1996) and 45–30 mya based on coccoliths (Cêpek in Schlee 1990). These are minimum dates, since most of the amber was secondarily deposited in turbid- itic sandstones of the Upper to Lower Miocene Mamey Group (Draper et al. 1994) and the length of time it took to re-deposit it is unknown. Observations and photographs were made with a Nikon SMZ- 10 R stereoscopic microscope and Nikon Optiphot compound Fig. 1. Extant pollinarium of L. attached to the mouth- parts of a honeybee (Apis mellifera: Apidae: Hymenoptera). C = corpus- microscope with magnifications up to 800 X. Helicon Focus Pro culum, T = translator arm; P = pollinium. X64 was used to stack photos for better clarity and depth of field.

52 American Entomologist • Spring 2017 Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021

Fig. 2. Lateral view of holotype of Discoflorus neotropicus gen. & sp. n. in Dominican amber. C = hirsute basal portion of coronal column; L = tips of coronal scales; T = termite. Scale bar = 1.8 mm.

Fig. 4. A. Gynostegium of Discoflorus neotropicus gen. & sp. n. in Domin- ican amber showing the ten-lobed stigmatic disk. Arrows show tips of three coronal scales. Scale bar = 0.6 mm. B. Diagrammatic drawing of Fig. 3. Bottom of holotype of Discoflorus neotropicus gen. & sp. n. the gynostegium of Discoflorus neotropicus gen. & sp. n. showing the in Dominican amber. C = calyx tube; Pe = peduncle, P = petal. Scale ten-lobed stigmatic disk (white), ten locules of the five anthers (black), bar = 1.2 mm. and tips of the ten corona scales (stippled).

Description Diagnosis. Flower perfect, actinomorphic, with a five-lobed Family Apocynaceae short calyx with sepals united at base, a five-parted rotate corolla Subfamily Asclepiadoideae with five equal to subequal, separate petals, five fertile with bilocular, broadly oblong anthers adherent to a ten-lobed Discoflorus gen. n. stigmatic disk and a ten-scaled coronal tube forming a gynoste- Type : Discoflorus neotropicus gen. n., sp. n. gium (Figs. 2-4). Locules of the five anthers positioned between Diagnosis: As for the type species (monotypic) every lobe of the stigmatic disk (Fig. 4). Tips of coronal scales are free, surround and barely surpass the peltate five-parted Discoflorus neotropicus gen. n., sp. n. (Figs. 2-9). stigma (Fig. 4). Pollinaria in stigmatic cavities were composed Etymology: The generic name is from the Latin “discora”= dif- of a corpusculum, translator arms and a fractured pollinium ferent and the Latin “floris” = blossom. Etymology—The spe- with some released pollen grains (Fig. 5). The slender corpus- cific epithet indicates the geographical location of the fossil. culum was sutured along the entire length of the outer surface. Type: Holotype in the Poinar amber collection maintained at Description. Flower perfect, small, with short calyx; sepals Oregon State University (Cat. No. Sd-9-46). united at base; corolla rotate, with five equal or subequal, sepa- Type locality: Amber mine (La Búcara) in the northern moun- rate petals with three reflexed and two upturned; stamens five, tain ranges (Cordillera Septentrional) of the Dominican anthers bilocular, broadly oblong, adherent with stigma head Republic (DD 19.4 by 70.4). and forming a gynostegium; corona composed of ten hirsute

American Entomologist • Volume 63, Number 1 53 column at base, 2.0 mm; length calyx 0.6 mm; length calyx lobes, 0.3-0.4 mm; length petals, 3.1-3.3 mm; width petals at base, 0.9-1.3 mm; diameter of stigma head, 1.4 mm; length of anthers, 340 µm; length pollinium translator arm, 90 µm; length corpuscula, 90-120 µm; greatest dimension of pollinium on termite head, 223 µm; diameter of pollen grains, 18-22 µm. Associated termite. A pollinarium with four pollinia is attached to the head of a 5 mm worker forager termite (Ter- mitidae: Isoptera) adjacent to the flower (Fig. 6). The corpus- culum is attached to the labrum and four adjacent pollinia are resting on the post-clypeus (Figs. 7-10). Pollinia size and shape vary greatly in the Asclepiadoideae; however, features of the fossil pollinia fall within the range of those depicted in

Swarupanandan et al. (1996). The size and shape of the cor- Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 puscula and the diameter of the pollen grains in the flower head are similar to those on the termite, and the pollinaria on the termite are considered to have originated from Discoflorus neotropicus gen. & sp. n. While two intact pollinia are clearly Fig. 5. Detail of corpusculum (C), part of translator arm (T), and pollen visible on the post-clypeus of the termite (Figs. 6-8), the outer grains (P) from a ruptured pollinium in the stigmatic chamber of Disco- two are broken and reduced in size (Fig. 9). florus neotropicus gen. & sp. n. in Dominican amber. Scale bar = 95 µm. Remarks. Of the nine extant genera of asclepiads in Hispan- iola (Liogier 1994), Discoflorus neotropicusgen. & sp. n. most scales mostly united into a column that surrounds the filaments closely resembles members of the R. Br., and gynoecium. Tips of coronal scales free, surrounding and in particular M. parviflorium (Sw.) Roem. & Schult. that has barely surpassing the peltate five-parted stigma. Stigma disk small flowers, a long-stipitate gynostegium and linear-spat- ten-lobed with locules of the five anthers positioned between ulate corona scales as long as the gynostegium. However, in every lobe. Ovary and style hidden from view. Metastelma, the corona has only five scales and the stigmatic Floral measurements. Length entire flower, 2.7 mm; length disk (gynostegium) is five-lobed, which is the normal condi- peduncle, 1.6 mm, length united portion of coronal column, tion in flowers of the Asclepiadoideae (Endress and Bruyns 1.8 mm; length free portion of coronal scales, 1.0 mm; width 2000; Endress 1994). In Discoflorus neotropicus gen. & sp. n.,

Fig. 6. Forager termite adjacent to the flower of Discoflorus neotropi- Fig. 7. Dorsal view of head of forager termite with two attached pol- cus gen. & sp. n. in Dominican amber. Arrow shows location of pollinia linia (P) of Discoflorus neotropicus gen. & sp. n. in Dominican amber. attached to termite head. Scale bar = 0.8 mm. Scale bar = 0.37 mm.

54 American Entomologist • Spring 2017 Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021

Fig. 9. Detail of four pollinia (arrows) of Discoflorus neotropicus gen. & sp. n. attached to termite head in Dominican amber. The two inner pol- linia are entire, but the two outer pollinia are partial. Scale bar = 130 µm.

Fig. 8. Frontal view of forager termite in Dominican amber with two attached entire pollinia (P) of Discoflorus neotropicus gen. & sp. n. P = pollinia. Scale bar = 0.20 mm. the corona is composed of ten scales and the stigmatic disk is ten-lobed (Fig. 4). The combination of small flower size, sepa- rate petals, a ten-lobed stigmatic disk and a ten-scaled coronal tube separate Discoflorus neotropicus gen. & sp. n. from extant Fig. 10. Detail of an entire pollinium of Discoflorus neotropicus gen. & sp. members of the Asclepiadoideae (Endress and Bruyns 2000). n. in Dominican amber. Arrow shows pollen grains. Scale bar = 70 µm.

Discussion material back to the nest (Hogue 1993, Hingston 1932). Mem- Based on fossil and molecular data, Rapini et al. (2007) cali- bers of the Termitidae comprise the majority of the 62 genera brated the Apocynaceae crown group to have appeared at the and 408 species of Neotropical termites and are part of the Paleocene/Eocene boundary (54 mya). However, the fossil record Dominican amber biota (Poinar and Poinar 1999). of the Asclepiadoideae is extremely meager, and represented In contrast to ants, the behavior of foraging termites is little only by a putative leaf impression in Baltic amber (Conwentz known, partly due to their small size and secretive habits. It is 1886) and putative pollen records in Old World mid-Oligocene likely that Neotropical termites harvest plant products mostly deposits (Muller 1981). Discoflorus neotropicus gen. & sp. n. is at night, similar to the harvesting behavior of Macrotermes spp. the first fossil flower of the Apocynaceae and not only provides workers in Africa (Lepage 1983). evidence of morphological variation of asclepiad flowers in the Since the fossil termite is not winged, it is assumed that it mid-Tertiary not known to occur in extant milkweed flowers, was visiting the flower of Discoflorus neotropicus gen. & sp. n. but establishes termites as pollinators of this early plant lineage. when both fell together into the resin. Many extant asclepiads Extant asclepiads are pollinated by Diptera, Coleoptera, produce nectar along the edge of the stigmatic disk (Woodson Hymenoptera, Hemiptera, and Lepidoptera (Woodson 1954; 1954) and the fossil termite may have been searching for nectar, Ollerton and Liede 1997; Wilson and Bertin 1979). There are which would explain how it acquired the pollinia. no previous reports of termites serving as pollinators of the Asclepiadoideae. However, Australian harvester termites of Acknowledgments the genus Drepanotermes (Termitidae) carry pollinaria of the Thanks are extended to Alessandro Rapini and Jeff Ollerton subterranean orchid, Rhizanthella gardneri R. S. Rogers (Epi- for providing literature and discussing characters of the fossil dendroideae) and are considered to be regular pollinators of flower and to Roberta Poinar for comments on earlier versions this orchid species (Dixon et al. 1990). This shows that some of the manuscript. termites do visit flowers, presumably for nectar. Worker termites of the family Termitidae, to which both the References Cited Australian Drepanotermes and the present fossil belong, are Conwentz, H. 1886. Die Angiospermen des Bernsteins, pp. 1-140. called “harvesters” because they search for and carry plant In Göppert H. R. and A. Menge (eds.). Die Flora des Bernstein

American Entomologist • Volume 63, Number 1 55 und ihre Beziehungen zur Flora der Tertiarformation und der Biological Journal of the Linnean Society 62: 593-610. Gegenwart, Vol. 2. Englemann, Danzig. Poinar, Jr., G.O. 1991. Hymenaea protera sp. n. (Leguminosae: Cae- Dixon, K.W., J.S. Pate, and J. Kuo, 1990. Th e Western Australian salpinioideae) from Dominican amber has African affi nities. Ex- fully subterranean orchid, Rhizanthella gardneri, pp. 37-62. In J. perientia 47:1075-1082. Arditti, (ed.). Orchid biology, reviews and perspectives 5. Timber Poinar, Jr., G.O., and R. Poinar 1999. Th e amber forest. Princeton Press, Portland, Oregon. University Press, Princeton, New Jersey, U.S.A. Draper, G., P. Mann, and J.F. Lewis. 1994. Hispaniola, pp. 129–150. Poinar, Jr. G.O. 2016a. Orchid pollinaria () attached In Donovan, S. and T.A Jackson, (eds.). Caribbean geology: an to stingless bees (Hymenoptera: Apidae) in Dominican amber. introduction. Th e University of the West Indies Publishers’ As- Neues Jahrbuch für Geologie und Paläontologie 279: 287-293. sociation. Kingston, Jamaica. Poinar, Jr. G.O. 2016b. Beetles with orchid pollinaria in Dominican Dressler, R.L. 1993. Phylogeny and Classifi cation of the orchid fam- and Mexican amber. American Entomologist 62: 172- 177. ily. Dioscorides Press, Portland, 314 pp. Rapini, A., C. van den Berg, and S. Liede-Schumann. 2007. Diver- Endress, M.E., and P.V. Bruyns. 2000. A revised classifi cation of the sifi cation of Asclepiadoideae (Apocynaceae) in the New World. Apocynaceae s. l. Th e Botanical Review 66: 1-57. Annals of the Missouri Botanical Garden 94: 407-422. Endress, P.K. 1994. Diversity and evolutionary biology of tropical Schlee, D. 1990. Das Bernstein-Kabinett. Stuttgarter Beiträge zur Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 fl owers. Cambridge University Press, Cambridge, 511 pp. Naturkunde. Ser. C, 28: 1-100. Hingston, R.W.G. 1932. A Naturalist in the Guiana Forest. Long- Swarupanandan, K., J.K. Mangaly, T.K. Sonny, K. Kishorekumar, mans, Green & Co., New York, 384 pp. and S.C. Basha. 1996. Th e subfamilial and tribal classifi cation Hogue, C.L. 1993. Latin American insects and Entomology. Univer- of the family Asclepiadaceae. Botanical Journal of the Linnean sity of California Press, Berkeley, 536 pp. Society 120: 327-369. Iturralde-Vinent, M.A., and R.D.E. MacPhee. 1996. Age and paleo- Wilson, M.F., and R.I. Bertin. 1979. Flower visitors, nectar produc- geographic origin of Dominican amber. Science 273:1850–1852. tion and infl orescence size of Asclepias syriaca L. Canadian Jour- Lepage, M.G. 1983. Foraging of Macrotermes spp. (Isoptera: Mac- nal of Botany 57: 1380-1388. rotermitinae) in the Tropics, pp. 205-218. In Jaission, P. (ed.). Woodson, R.E. 1954. Th e North American species of Asclepias L. Social insects in the Tropics. Vol. 2. Université Paris-nord, Paris. Annals of the Missouri Botanical Garden 41:1-211. Liogier, A.H. 1994. La fl ora de la Española. VI. San Pedro de Ma- coris, Dominican Republic, 517 pp. George Poinar Jr. ([email protected]) has studied a variety of organisms, from microbes to vertebrates, in amber deposits around the Fossil pollen records of extant angiosperms. Th e Muller, J. 1981. world. He is especially interested in pathogens associated with blood-suck- Botanical Review 47: 1–142. ing arthropods and associations between insects and flowers. Ollerton, J., and S. Liede. 1997. Th e evolution of pollination sys- tems in the Asclepiadaceae: a survey and preliminary analysis. DOI: 10.1093/ae/tmx011

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